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Transcriptional profiles of bovine in vivo pre-implantation development
During mammalian pre-implantation embryonic development dramatic and orchestrated changes occur in gene transcription. The identification of the complete changes has not been possible until the development of the Next Generation Sequencing Technology. Here we report comprehensive transcriptome dynam...
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Published in: | BMC genomics 2014-09, Vol.15 (1), p.756-756, Article 756 |
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creator | Jiang, Zongliang Sun, Jiangwen Dong, Hong Luo, Oscar Zheng, Xinbao Obergfell, Craig Tang, Yong Bi, Jinbo O'Neill, Rachel Ruan, Yijun Chen, Jingbo Tian, Xiuchun Cindy |
description | During mammalian pre-implantation embryonic development dramatic and orchestrated changes occur in gene transcription. The identification of the complete changes has not been possible until the development of the Next Generation Sequencing Technology.
Here we report comprehensive transcriptome dynamics of single matured bovine oocytes and pre-implantation embryos developed in vivo. Surprisingly, more than half of the estimated 22,000 bovine genes, 11,488 to 12,729 involved in more than 100 pathways, is expressed in oocytes and early embryos. Despite the similarity in the total numbers of genes expressed across stages, the nature of the expressed genes is dramatically different. A total of 2,845 genes were differentially expressed among different stages, of which the largest change was observed between the 4- and 8-cell stages, demonstrating that the bovine embryonic genome is activated at this transition. Additionally, 774 genes were identified as only expressed/highly enriched in particular stages of development, suggesting their stage-specific roles in embryogenesis. Using weighted gene co-expression network analysis, we found 12 stage-specific modules of co-expressed genes that can be used to represent the corresponding stage of development. Furthermore, we identified conserved key members (or hub genes) of the bovine expressed gene networks. Their vast association with other embryonic genes suggests that they may have important regulatory roles in embryo development; yet, the majority of the hub genes are relatively unknown/under-studied in embryos. We also conducted the first comparison of embryonic expression profiles across three mammalian species, human, mouse and bovine, for which RNA-seq data are available. We found that the three species share more maternally deposited genes than embryonic genome activated genes. More importantly, there are more similarities in embryonic transcriptomes between bovine and humans than between humans and mice, demonstrating that bovine embryos are better models for human embryonic development.
This study provides a comprehensive examination of gene activities in bovine embryos and identified little-known potential master regulators of pre-implantation development. |
doi_str_mv | 10.1186/1471-2164-15-756 |
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Here we report comprehensive transcriptome dynamics of single matured bovine oocytes and pre-implantation embryos developed in vivo. Surprisingly, more than half of the estimated 22,000 bovine genes, 11,488 to 12,729 involved in more than 100 pathways, is expressed in oocytes and early embryos. Despite the similarity in the total numbers of genes expressed across stages, the nature of the expressed genes is dramatically different. A total of 2,845 genes were differentially expressed among different stages, of which the largest change was observed between the 4- and 8-cell stages, demonstrating that the bovine embryonic genome is activated at this transition. Additionally, 774 genes were identified as only expressed/highly enriched in particular stages of development, suggesting their stage-specific roles in embryogenesis. Using weighted gene co-expression network analysis, we found 12 stage-specific modules of co-expressed genes that can be used to represent the corresponding stage of development. Furthermore, we identified conserved key members (or hub genes) of the bovine expressed gene networks. Their vast association with other embryonic genes suggests that they may have important regulatory roles in embryo development; yet, the majority of the hub genes are relatively unknown/under-studied in embryos. We also conducted the first comparison of embryonic expression profiles across three mammalian species, human, mouse and bovine, for which RNA-seq data are available. We found that the three species share more maternally deposited genes than embryonic genome activated genes. More importantly, there are more similarities in embryonic transcriptomes between bovine and humans than between humans and mice, demonstrating that bovine embryos are better models for human embryonic development.
This study provides a comprehensive examination of gene activities in bovine embryos and identified little-known potential master regulators of pre-implantation development.</description><identifier>ISSN: 1471-2164</identifier><identifier>EISSN: 1471-2164</identifier><identifier>DOI: 10.1186/1471-2164-15-756</identifier><identifier>PMID: 25185836</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Analysis ; Animal sciences ; Animals ; Blastocyst - metabolism ; Cattle ; Chromosome Mapping ; Cluster Analysis ; Colleges & universities ; Computational Biology ; Embryonic Development - genetics ; Female ; Gene expression ; Gene Expression Profiling ; Gene Expression Regulation, Developmental ; Gene Regulatory Networks ; Genes ; Genetic aspects ; Genomes ; Humans ; Methods ; Mice ; Ontology ; Oocytes - metabolism ; Pregnancy ; Principal components analysis ; Reproducibility of Results ; RNA polymerase ; Transcriptome ; Zoology</subject><ispartof>BMC genomics, 2014-09, Vol.15 (1), p.756-756, Article 756</ispartof><rights>COPYRIGHT 2014 BioMed Central Ltd.</rights><rights>2014 Jiang et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.</rights><rights>Jiang et al.; licensee BioMed Central Ltd. 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-b684t-78eda0ad1a9e8952b7fc869f6e7569b34a0b4326e097ca2c4ae4df958aee74683</citedby><cites>FETCH-LOGICAL-b684t-78eda0ad1a9e8952b7fc869f6e7569b34a0b4326e097ca2c4ae4df958aee74683</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4162962/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1561362478?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25752,27923,27924,37011,37012,44589,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25185836$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jiang, Zongliang</creatorcontrib><creatorcontrib>Sun, Jiangwen</creatorcontrib><creatorcontrib>Dong, Hong</creatorcontrib><creatorcontrib>Luo, Oscar</creatorcontrib><creatorcontrib>Zheng, Xinbao</creatorcontrib><creatorcontrib>Obergfell, Craig</creatorcontrib><creatorcontrib>Tang, Yong</creatorcontrib><creatorcontrib>Bi, Jinbo</creatorcontrib><creatorcontrib>O'Neill, Rachel</creatorcontrib><creatorcontrib>Ruan, Yijun</creatorcontrib><creatorcontrib>Chen, Jingbo</creatorcontrib><creatorcontrib>Tian, Xiuchun Cindy</creatorcontrib><title>Transcriptional profiles of bovine in vivo pre-implantation development</title><title>BMC genomics</title><addtitle>BMC Genomics</addtitle><description>During mammalian pre-implantation embryonic development dramatic and orchestrated changes occur in gene transcription. The identification of the complete changes has not been possible until the development of the Next Generation Sequencing Technology.
Here we report comprehensive transcriptome dynamics of single matured bovine oocytes and pre-implantation embryos developed in vivo. Surprisingly, more than half of the estimated 22,000 bovine genes, 11,488 to 12,729 involved in more than 100 pathways, is expressed in oocytes and early embryos. Despite the similarity in the total numbers of genes expressed across stages, the nature of the expressed genes is dramatically different. A total of 2,845 genes were differentially expressed among different stages, of which the largest change was observed between the 4- and 8-cell stages, demonstrating that the bovine embryonic genome is activated at this transition. Additionally, 774 genes were identified as only expressed/highly enriched in particular stages of development, suggesting their stage-specific roles in embryogenesis. Using weighted gene co-expression network analysis, we found 12 stage-specific modules of co-expressed genes that can be used to represent the corresponding stage of development. Furthermore, we identified conserved key members (or hub genes) of the bovine expressed gene networks. Their vast association with other embryonic genes suggests that they may have important regulatory roles in embryo development; yet, the majority of the hub genes are relatively unknown/under-studied in embryos. We also conducted the first comparison of embryonic expression profiles across three mammalian species, human, mouse and bovine, for which RNA-seq data are available. We found that the three species share more maternally deposited genes than embryonic genome activated genes. More importantly, there are more similarities in embryonic transcriptomes between bovine and humans than between humans and mice, demonstrating that bovine embryos are better models for human embryonic development.
This study provides a comprehensive examination of gene activities in bovine embryos and identified little-known potential master regulators of pre-implantation development.</description><subject>Analysis</subject><subject>Animal sciences</subject><subject>Animals</subject><subject>Blastocyst - metabolism</subject><subject>Cattle</subject><subject>Chromosome Mapping</subject><subject>Cluster Analysis</subject><subject>Colleges & universities</subject><subject>Computational Biology</subject><subject>Embryonic Development - genetics</subject><subject>Female</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Gene Regulatory Networks</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Humans</subject><subject>Methods</subject><subject>Mice</subject><subject>Ontology</subject><subject>Oocytes - metabolism</subject><subject>Pregnancy</subject><subject>Principal components analysis</subject><subject>Reproducibility of Results</subject><subject>RNA polymerase</subject><subject>Transcriptome</subject><subject>Zoology</subject><issn>1471-2164</issn><issn>1471-2164</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><recordid>eNqNkt9r1TAUx4s43Nx890kKvriHziTNzxdhXNwcDATdnkOanl4z2qYmbZn_vSl3XtcxQfKQkPM533z5nmTZW4zOMJb8I6YCFwRzWmBWCMZfZEf7q5ePzofZ6xjvEMJCEvYqOyQMSyZLfpRd3gTTRxvcMDrfmzYfgm9cCzH3TV752fWQuz6f3exTCQrXDa3pR7PQeQ0ztH7ooB9PsoPGtBHePOzH2e3F55vNl-L66-XV5vy6qLikYyEk1AaZGhsFUjFSicZKrhoOyb2qSmpQRUvCASlhDbHUAK0bxaQBEJTL8jj7tNMdpqqD2qang2n1EFxnwi_tjdPrSu9-6K2fNcWcKE6SwGYnUDn_D4F1xfpOL0HqJUiNmU5Ok8qHBxvB_5wgjrpz0UKbsgE_xYRxLonCSP4PipUgKYyEvn-C3vkppKnsqJITKuRfamta0K5vfPJpF1F9zkrFOJOiTNTZM1RaNXTO-h6WKa8bTlcNiRnhftyaKUZ99f3bmkU71gYfY4Bmnx9GevmZzyX27vHg9g1_vmL5G9Q13UI</recordid><startdate>20140904</startdate><enddate>20140904</enddate><creator>Jiang, Zongliang</creator><creator>Sun, Jiangwen</creator><creator>Dong, Hong</creator><creator>Luo, Oscar</creator><creator>Zheng, Xinbao</creator><creator>Obergfell, Craig</creator><creator>Tang, Yong</creator><creator>Bi, Jinbo</creator><creator>O'Neill, Rachel</creator><creator>Ruan, Yijun</creator><creator>Chen, Jingbo</creator><creator>Tian, Xiuchun Cindy</creator><general>BioMed Central Ltd</general><general>BioMed Central</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISR</scope><scope>3V.</scope><scope>7QP</scope><scope>7QR</scope><scope>7SS</scope><scope>7TK</scope><scope>7U7</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>RC3</scope><scope>7X8</scope><scope>7QO</scope><scope>5PM</scope></search><sort><creationdate>20140904</creationdate><title>Transcriptional profiles of bovine in vivo pre-implantation development</title><author>Jiang, Zongliang ; Sun, Jiangwen ; Dong, Hong ; Luo, Oscar ; Zheng, Xinbao ; Obergfell, Craig ; Tang, Yong ; Bi, Jinbo ; O'Neill, Rachel ; Ruan, Yijun ; Chen, Jingbo ; Tian, Xiuchun Cindy</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-b684t-78eda0ad1a9e8952b7fc869f6e7569b34a0b4326e097ca2c4ae4df958aee74683</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Analysis</topic><topic>Animal sciences</topic><topic>Animals</topic><topic>Blastocyst - metabolism</topic><topic>Cattle</topic><topic>Chromosome Mapping</topic><topic>Cluster Analysis</topic><topic>Colleges & universities</topic><topic>Computational Biology</topic><topic>Embryonic Development - genetics</topic><topic>Female</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Gene Regulatory Networks</topic><topic>Genes</topic><topic>Genetic aspects</topic><topic>Genomes</topic><topic>Humans</topic><topic>Methods</topic><topic>Mice</topic><topic>Ontology</topic><topic>Oocytes - metabolism</topic><topic>Pregnancy</topic><topic>Principal components analysis</topic><topic>Reproducibility of Results</topic><topic>RNA polymerase</topic><topic>Transcriptome</topic><topic>Zoology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jiang, Zongliang</creatorcontrib><creatorcontrib>Sun, Jiangwen</creatorcontrib><creatorcontrib>Dong, Hong</creatorcontrib><creatorcontrib>Luo, Oscar</creatorcontrib><creatorcontrib>Zheng, Xinbao</creatorcontrib><creatorcontrib>Obergfell, Craig</creatorcontrib><creatorcontrib>Tang, Yong</creatorcontrib><creatorcontrib>Bi, Jinbo</creatorcontrib><creatorcontrib>O'Neill, Rachel</creatorcontrib><creatorcontrib>Ruan, Yijun</creatorcontrib><creatorcontrib>Chen, Jingbo</creatorcontrib><creatorcontrib>Tian, Xiuchun Cindy</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Biotechnology Research Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>BMC genomics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jiang, Zongliang</au><au>Sun, Jiangwen</au><au>Dong, Hong</au><au>Luo, Oscar</au><au>Zheng, Xinbao</au><au>Obergfell, Craig</au><au>Tang, Yong</au><au>Bi, Jinbo</au><au>O'Neill, Rachel</au><au>Ruan, Yijun</au><au>Chen, Jingbo</au><au>Tian, Xiuchun Cindy</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Transcriptional profiles of bovine in vivo pre-implantation development</atitle><jtitle>BMC genomics</jtitle><addtitle>BMC Genomics</addtitle><date>2014-09-04</date><risdate>2014</risdate><volume>15</volume><issue>1</issue><spage>756</spage><epage>756</epage><pages>756-756</pages><artnum>756</artnum><issn>1471-2164</issn><eissn>1471-2164</eissn><abstract>During mammalian pre-implantation embryonic development dramatic and orchestrated changes occur in gene transcription. The identification of the complete changes has not been possible until the development of the Next Generation Sequencing Technology.
Here we report comprehensive transcriptome dynamics of single matured bovine oocytes and pre-implantation embryos developed in vivo. Surprisingly, more than half of the estimated 22,000 bovine genes, 11,488 to 12,729 involved in more than 100 pathways, is expressed in oocytes and early embryos. Despite the similarity in the total numbers of genes expressed across stages, the nature of the expressed genes is dramatically different. A total of 2,845 genes were differentially expressed among different stages, of which the largest change was observed between the 4- and 8-cell stages, demonstrating that the bovine embryonic genome is activated at this transition. Additionally, 774 genes were identified as only expressed/highly enriched in particular stages of development, suggesting their stage-specific roles in embryogenesis. Using weighted gene co-expression network analysis, we found 12 stage-specific modules of co-expressed genes that can be used to represent the corresponding stage of development. Furthermore, we identified conserved key members (or hub genes) of the bovine expressed gene networks. Their vast association with other embryonic genes suggests that they may have important regulatory roles in embryo development; yet, the majority of the hub genes are relatively unknown/under-studied in embryos. We also conducted the first comparison of embryonic expression profiles across three mammalian species, human, mouse and bovine, for which RNA-seq data are available. We found that the three species share more maternally deposited genes than embryonic genome activated genes. More importantly, there are more similarities in embryonic transcriptomes between bovine and humans than between humans and mice, demonstrating that bovine embryos are better models for human embryonic development.
This study provides a comprehensive examination of gene activities in bovine embryos and identified little-known potential master regulators of pre-implantation development.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>25185836</pmid><doi>10.1186/1471-2164-15-756</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Analysis Animal sciences Animals Blastocyst - metabolism Cattle Chromosome Mapping Cluster Analysis Colleges & universities Computational Biology Embryonic Development - genetics Female Gene expression Gene Expression Profiling Gene Expression Regulation, Developmental Gene Regulatory Networks Genes Genetic aspects Genomes Humans Methods Mice Ontology Oocytes - metabolism Pregnancy Principal components analysis Reproducibility of Results RNA polymerase Transcriptome Zoology |
title | Transcriptional profiles of bovine in vivo pre-implantation development |
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